Retinoic Acid Inhibits Rat XY Gonad Development by Blocking Mesonephric Cell Migration and Decreasing the Number of Gonocytes

Biology of Reproduction

Volumn 70, Issue 3, 2004, Pages 687-693

  Li, Hui ^a   Kim, Kwan Hee ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Embryo; Gamete biology; Sertoli cells; Steroid hormone receptors; Testis

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; MUELLERIAN INHIBITING FACTOR; RETINOIC ACID; RETINOIC ACID DERIVATIVE; RETINOIC ACID RECEPTOR ALPHA; RETINOL; RO 41 5253; STEROID HORMONE ANTAGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION; GONAD DEVELOPMENT; KNOCKOUT MOUSE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RETINOL DEFICIENCY; SERTOLI CELL; SPERMATOGENESIS; TESTIS FUNCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; GLYCOPROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MESONEPHROS; ORGAN CULTURE TECHNIQUES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, RETINOIC ACID; SERTOLI CELLS; TESTICULAR HORMONES; TESTIS; TRETINOIN;

ANIMALIA; MAMMALIA; RODENTIA;

EID: 1242276445     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.023135     Document Type: Article

References (52)

1. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991; 351:117-121.
2. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990; 346:240-244.
3. Buehr M, Gu S, McLaren A. Mesonephric contribution to testis differentiation in the fetal mouse. Development 1993; 117:273-281.
4. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B. Male-specific cell migration into the developing gonad. Curr Biol 1997; 7:958-968.
5. Magre S, Jost A. The initial phases of testicular organogenesis in the rat. An electron microscope study. Arch Anat Microsc Morphol Exp 1980; 69:297-318.
6. Jost A, Magre S, Agelopoulou R. Early stages of testicular differentiation in the rat. Hum Genet 1981; 58:59-63.
7. Magre S, Jost A. Sertoli cells and testicular differentiation in the rat fetus. J Electron Microsc Technol 1991; 19:172-188.
8. Josso N, Picard JY. Anti-Mullerian hormone. Physiol Rev 1986; 66:1038-1090.
9. Josso N, Cate RL, Picard JY, Vigier B, di Clemente N, Wilson C, Imbeaud S, Pepinsky RB, Guerrier D, Boussin L, Legeai L, Carre-Eusebe D. Anti-Mullerian hormone: the Jost factor. Recent Prog Horm Res 1993; 48:1-59.
10. Behringer RR. The Mullerian inhibitor and mammalian sexual development. Philos Trans R Soc London B, Biol Sci 1995; 350:285-288.
11. Roberts LM, Hirokawa Y, Nachtigal MW, Ingraham HA. Paracrine-mediated apoptosis in reproductive tract development. Dev Biol 1999; 208:110-122.
12. Behringer RR, Finegold MJ, Cate RL. Mullerian-inhibiting substance function during mammalian sexual development. Cell 1994; 79:415-425.
13. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RR. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 1996; 10:2577-2587.
14. Chytil F. Retinoids in lung development. FASEB J 1996; 10:986-992.
15. Kim KH, Wang Z. Action of vitamin A on the testis: role of the Sertoli cell. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:517-536.
16. Maden M. Vitamin A in embryonic development. Nutr Rev 1994; 52:S3-12.
17. Sulik KK, Cook CS, Webster WS. Teratogens and craniofacial malformations: relationship to cell death. Development 1988; 103(suppl):213-231.
18. Mason KE. Differences in testes injury and repair after vitamin deficiency, vitamin E deficiency and inanition. Am J Anat 1933; 52:153-239.
19. Mitranond V, Sobhon P, Tosukhowong P, Chindaduangrat W. Cytological changes in the testes of vitamin A-deficient rats. I. Quantitation of germinal cells in the seminiferous tubules. Acta Anat (Basel) 1979; 103:159-168.
20. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996; 10:940-954.
21. Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell 1995; 83:841-850.
22. Pfahl M, Chytil F. Regulation of metabolism by retinoic acid and its nuclear receptors. Annu Rev Nutr 1996; 16:257-283.
23. Giguere V. Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr Rev 1994; 15:61-79.
24. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M, Chambon P. High postnatal lethality and testis degeneration in retinoic acid receptor α mutant mice. Proc Natl Acad Sci U S A 1993; 90:7225-7229.
25. Kastner P, Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Decimo D, Krezel W, Dierich A, Chambon P. Abnormal spermatogenesis in RXR-β mutant mice. Genes Dev 1996; 10:80-92.
26. Huang HF, Dyrenfurth I, Hembree WC. Endocrine changes associated with germ cell loss during vitamin A-induced recovery of spermatogenesis. Endocrinology 1983; 112:1163-1171.
27. Van Pelt AM, de Rooij DG. Retinoic acid is able to reinitiate spermatogenesis in vitamin A deficient rats and high replicate doses support the full development of spermatogenic cell. Endocrinology 1991; 128:697-704.
28. Cupp AS, Dufour JM, Kim G, Skinner MK, Kim KH. Action of retinoids on embryonic and early postnatal testis development. Endocrinology 1999; 140:2343-2352.
29. Livera G, Rouiller-Fabre V, Pairault C, Levacher C, Habert R. Regulation and perturbation of testicular functions by vitamin A. Reproduction 2002; 124:173-180.
30. Marinos E, Kulukussa M, Zotos A, Kittas C. Retinoic acid affects basement membrane formation of the seminiferous cords in 14-day male rat gonads in vitro. Differentiation 1995; 59:87-94.
31. Szondy Z, Reichert U, Bernardon JM, Michel S, Toth R, Karaszi E, Fesus L. Inhibition of activation-induced apoptosis of thymocytes by all-trans- and 9-cis-retinoic acid is mediated via retinoic acid receptor alpha. Biochem J 1998; 331:767-774.
32. Livera G, Rouiller-Fabre V, Habert R. Retinoid receptors involved in the effects of retinoic acid on rat testis development. Biol Reprod 2001; 64:1307-1314.
33. Apfel C, Bauer F, Crettaz M, Forni L, Kamber M, Kaufmann F, LeMotte P, Pirson W, Klaus M. A retinoic acid receptor alpha antagonist selectively counteracts retinoic acid effects. Proc Natl Acad Sci U S A 1992; 89:7129-7133.
34. Cupp AS, Uzumcu M, Skinner MK. Chemotactic role of neurotropin 3 in the embryonic testis that facilitates male sex determination. Biol Reprod 2003; 68:2033-2037.
35. Uzumcu M, Westfall SD, Dirks KA, Skinner MK. Embryonic testis cord formation and mesonephric cell migration requires the phosphatidylinositol 3-kinase signaling pathway. Biol Reprod 2002; 67:1927-1935.
36. Dufour JM, Kim KH. Cellular and subcellular localization of six retinoid receptors in rat testis during postnatal development: identification of potential heterodimeric receptors. Biol Reprod 1999; 61:1300-1308.
37. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 2000; 93:139-149.
38. Tilmann C, Capel B. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 1999; 126:2883-2890.
39. Munsterberg A, Lovell-Badge R. Expression of the mouse anti-Mullerian hormone gene suggests a role in both male and female sexual differentiation. Development 1991; 113:613-624.
40. Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001; 104:875-889.
41. Capel B. The battle of the sexes. Mech Dev 2000; 92:89-103.
42. Burgoyne PS, Buehr M, Koopman P, Rossant J, McLaren A. Cell-autonomous action of the testis-determining gene: Sertoli cells are exclusively XY in XX ↔ XY chimeric mouse testes. Development 1988; 102:443-450.
43. Albrecht KH, Eicher EM. Evidence that Sry is expressed in preSertoli cells and Sertoli and granulosa cells have a common precursor. Dev Biol 2001; 240:92-107.
44. Skinner MK, Tung PS, Fritz IB. Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 1985; 100:1941-1947.
45. Tung PS, Fritz IB. Morphogenetic restructuring and formation of basement membranes by Sertoli cells and testis peritubular cells in coculture: inhibition of the morphogenetic cascade by cyclic AMP derivatives and by blocking direct cell contact. Dev Biol 1987; 120:139-153.
46. Capel B, Albrecht KH, Washburn LL, Eicher EM. Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech Dev 1999; 84:127-131.
47. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 2000; 163:3-9.
48. de Rooij DG, Grootegoed JA. Spermatogonial stem cells. Curr Opin Cell Biol 1998; 10:694-701.
49. Orth JM, Jester WF, Li LH, Laslett AL. Gonocyte-Sertoli cell interactions during development of the neonatal rodent testis. Curr Top Dev Biol 2000; 50:103-124.
50. Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y. Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 2000; 258:210-220.
51. Merchant H. Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol 1975; 44:1-21.
52. Livera G, Rouiller-Fabre V, Durand P, Habert R. Multiple effects of retinoids on the development of Sertoli, germ, and Leydig cells of fetal and neonatal rat testis in culture. Biol Reprod 2000; 62:1303-1314.